Advances in the Regulatory Mechanisms of Pollen Response to Heat Stress in Crops

doi:10.11983/CBB18133

Abstract

Abstract: As a consequence of global warming, crops face more acute and more frequent high-temperature stress. Heat threatens the whole plant development, especially pollen development, which seems to be the most sensitive process in the plant life cycle. Hence, the mechanism underlying the pollen response to heat stress has become a hot topic in the field of plant biology. Recent studies have revealed that pollen has at least 4 ways to perceive the heat stress signal: calcium channels, unfolded protein response, reactive oxygen species and H2A.Z. Pollen responds to heat stress by regulating heat shock protein expression, glycol-metabolism and phytohormone level and enhancing reactive oxygen species scavenging capacity. In this review, we summarize pollen development defects under heat stress, the mechanism of pollen thermotolerance and discuss how to design the experiments to study pollen thermotolerance. The overview provides guidelines for the pollen heat response mechanism in crops.

Key words: crop, pollen, heat, response mechanism

Hao Yang, Chen Liu, Zhifei Wang, Xiuli Hu, Tai Wang. Advances in the Regulatory Mechanisms of Pollen Response to Heat Stress in Crops[J]. Chinese Bulletin of Botany, 2019, 54(2): 157-167.

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URL: https://www.chinbullbotany.com/EN/10.11983/CBB18133

https://www.chinbullbotany.com/EN/Y2019/V54/I2/157

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References 105

[1]	鲁云龙, 魏丽勤, 戴绍军, 王台 ( 2014). 被子植物生殖细胞与精细胞的分离方法. 植物学报 49, 229-245. DOI URL
[2]	Arshad MS, Farooq M, Asch F, Krishna JSV, Prasad PVV, Siddique KHM ( 2017). Thermal stress impacts reproduce- tive development and grain yield in rice. Plant Physiol Biochem 115, 57-72. DOI URL
[3]	Barnabás B, Jager K, Fehér A ( 2008). The effect of drought and heat stress on reproductive processes in cereals. Plant Cell Environ 31, 11-38. DOI URL PMID
[4]	Begcy K, Dresselhaus T ( 2017). Tracking maize pollen development by the Leaf Collar Method. Plant Reprod 30, 171-178. DOI URL PMID
[5]	Boden SA, Kavanova M, Finnegan EJ, Wigge PA ( 2013). Thermal stress effects on grain yield in Brachypodium distachyon occur via H2A.Z-nucleosomes . Genome Biol 14, R65.
[6]	Bokszczanin KL, Krezdorn N, Fragkostefanakis S, Müller S, Rycak L, Chen YY, Hoffmeier K, Kreutz J, Paupière MJ, Chaturvedi P, Iannacone R, Müller F, Bostan H, Chiusano ML, Scharf KD, Rotter B, Schleiff E, Winter P, SPOT-ITN Consortium ( 2015). Identification of novel small ncRNAs in pollen of tomato. BMC Genomics 16, 714. DOI URL PMID
[7]	Burke JJ, Chen JP ( 2015). Enhancement of reproductive heat tolerance in plants. PLoS One 10, e0122933. DOI URL PMID
[8]	Chaturvedi P, Doerfler H, Jegadeesan S, Ghatak A, Pressman E, Castillejo MA, Wienkoop S, Egelhofer V, Firon N, Weckwerth W ( 2015). Heat-treatment-responsive proteins in different developmental stages of tomato pollen detected by targeted mass accuracy precursor alignment (tMAPA). J Proteome Res 14, 4463-4471. DOI URL PMID
[9]	Chen YY, Müller F, Rieu I, Winter P ( 2016). Epigenetic events in plant male germ cell heat stress responses. Plant Reprod 29, 21-29. DOI URL
[10]	Coast O, Murdoch AJ, Ellis RH, Hay FR, Jagadish KS ( 2016). Resilience of rice ( Oryza spp.) pollen germination and tube growth to temperature stress. Plant Cell Environ 39, 26-37. DOI URL
[11]	Couée I, Sulmon C, Gouesbet G, El Amrani A ( 2006). Involvement of soluble sugars in reactive oxygen species balance and responses to oxidative stress in plants. J Exp Bot 57, 449-459. DOI URL PMID
[12]	De Storme N, Geelen D ( 2011). The Arabidopsis mutantjason produces unreduced first division restitution male gametes through a parallel/fused spindle mechanism in meiosis II. Plant Physiol 155, 1403-1415. DOI URL PMID
[13]	De Storme N, Geelen D ( 2014). The impact of environmental stress on male reproductive development in plants: biological processes and molecular mechanisms. Plant Cell Environ 37, 1-18. DOI URL PMID
[14]	Deng Y, Srivastava R, Quilichini TD, Dong HL, Bao Y, Horner HT, Howell SH ( 2016). IRE1, a component of the unfolded protein response signaling pathway, protects pollen development in Arabidopsis from heat stress. Plant J 88, 193-204. DOI URL PMID
[15]	d'Erfurth I, Jolivet S, Froger N, Catrice O, Novatchkova M, Simon M, Jenczewski E, Mercier R ( 2008). Mutations in AtPS1 (Arabidopsis thaliana parallel spindle 1) lead to the production of diploid pollen grains. PLoS Genet 4, e1000-274.
[16]	Ding YH, Ma YZ, Liu N, Xu J, Hu Q, Li YY, Wu YL, Xie S, Zhu LF, Min L, Zhang XL ( 2017). microRNAs involved in auxin signaling modulate male sterility under high-tem- perature stress in cotton (Gossypium hirsutum). Plant J 91, 977-994.
[17]	Draeger T, Moore G ( 2017). Short periods of high temperature during meiosis prevent normal meiotic progression and reduce grain number in hexaploid wheat (Triticum aestivum L.). Theor Appl Genet 130, 1785-1800. DOI URL PMID
[18]	Endo M, Tsuchiya T, Hamada K, Kawamura S, Yano K, Ohshima M, Higashitani A, Watanabe M, Kawagishi-Kobayashi M ( 2009). High temperatures cause male sterility in rice plants with transcriptional alterations during pollen development. Plant Cell Physiol 50, 1911-1922. DOI URL PMID
[19]	Endo S, Shinohara H, Matsubayashi Y, Fukuda H ( 2013). A novel pollen-pistil interaction conferring high-temperature tolerance during reproduction via CLE45 signaling. Curr Biol 23, 1670-1676. DOI URL PMID
[20]	Farooq M, Bramley H, Palta JA, Siddique KHM ( 2011). Heat stress in wheat during reproductive and grain-filling phases. Crit Rev Plant Sci 30, 491-507. DOI URL
[21]	Fernández-Bautista N, Fernández-Calvino L, Muñoz A, Castellano MM ( 2017). HOP3, a member of the HOP family in Arabidopsis, interacts with BiP and plays a major role in the ER stress response. Plant Cell Environ 40, 1341-1355. DOI URL PMID
[22]	Firon N, Pressman E, Meir S, Khoury R, Altahan L ( 2012). Ethylene is involved in maintaining tomato (Solanum lycopersicum) pollen quality under heat-stress conditions. AoB Plants 2012,pls024.
[23]	Firon N, Shaked R, Peet MM, Pharr DM, Zamski E, Rosenfeld K, Althan L, Pressman E ( 2006). Pollen grains of heat tolerant tomato cultivars retain higher carbohydrate concentration under heat stress conditions. Sci Hortic 109, 212-217. DOI URL
[24]	Fragkostefanakis S, Mesihovic A, Hu YJ, Schleiff E ( 2016a). Unfolded protein response in pollen development and heat stress tolerance. Plant Reprod 29, 81-91. DOI URL PMID
[25]	Fragkostefanakis S, Mesihovic A, Simm S, Paupière MJ, Hu YJ, Paul P, Mishra SK, Tschiersch B, Theres K, Bovy A, Schleiff E, Scharf KD ( 2016b). HsfA2 controls the activity of developmentally and stress-regulated heat stress protection mechanisms in tomato male reproductive tissues. Plant Physiol 170, 2461-2477. DOI URL PMID
[26]	Fragkostefanakis S, Röth S, Schleiff E, Scharf KD ( 2015). Prospects of engineering thermotolerance in crops through modulation of heat stress transcription factor and heat shock protein networks. Plant Cell Environ 38, 1881-1895. DOI URL PMID
[27]	Francis KE, Lam SY, Harrison BD, Bey AL, Berchowitz LE, Copenhaver GP ( 2007). Pollen tetrad-based visual assay for meiotic recombination in Arabidopsis. Proc Natl Acad Sci USA 104, 3913-3918. DOI URL
[28]	Frank G, Pressman E, Ophir R, Althan L, Shaked R, Freedman M, Shen S, Firon N ( 2009). Transcriptional profiling of maturing tomato (Solanum lycopersicum L.) microspores reveals the involvement of heat shock proteins, ROS scavengers, hormones, and sugars in the heat stress response. J Exp Bot 60, 3891-3908. DOI URL PMID
[29]	Gao F, Han XW, Wu JH, Zheng SZ, Shang ZL, Sun DY, Zhou RG, Li B ( 2012). A heat-activated calcium-perme- able channel—Arabidopsis cyclic nucleotide-gated ion channel 6—is involved in heat shock responses. Plant J 70, 1056-1069. DOI URL PMID
[30]	Giorno F, Wolters-Arts M, Grillo S, Scharf KD, Vriezen WH, Mariani C ( 2010). Developmental and heat stress- regulated expression of HsfA2 and small heat shock proteins in tomato anthers. J Exp Bot 61, 453-462. DOI URL PMID
[31]	González-Schain N, Dreni L, Lawas LMF, Galbiati M, Colombo L, Heuer S, Jagadish KSV, Kater MM ( 2016). Genome-wide transcriptome analysis during anthesis reveals new insights into the molecular basis of heat stress responses in tolerant and sensitive rice varieties. Plant Cell Physiol 57, 57-68. DOI URL PMID
[32]	Hansen G ( 2015). The evolution of the evidence base for observed impacts of climate change. Curr Opin Environ Sustain 14, 187-197. DOI URL
[33]	Higashitani A ( 2013). High temperature injury and auxin biosynthesis in microsporogenesis. Front Plant Sci 4, 47. DOI URL PMID
[34]	Hu LF, Liang WQ, Yin CS, Cui X, Zong J, Wang X, Hu JP, Zhang DB ( 2011). Rice MADS3 regulates ROS homeostasis during late anther development. Plant Cell 23, 515-533. DOI URL PMID
[35]	Jagadish SVK, Muthurajan R, Oane R, Wheeler TR, Heuer S, Bennett J, Craufurd PQ ( 2010). Physiological and proteomic approaches to address heat tolerance during anthesis in rice (Oryza sativa L.). J Exp Bot 61, 143-156. DOI URL PMID
[36]	Jain M, Chourey PS, Boote KJ, Allen Jr LH ( 2010). Short- term high temperature growth conditions during vegetative-to-reproductive phase transition irreversibly compromise cell wall invertase-mediated sucrose catalysis and microspore meiosis in grain sorghum (Sorghum bicolor). J Plant Physiol 167, 578-582. DOI URL PMID
[37]	Jegadeesan S, Beery A, Altahan L, Meir S, Pressman E, Firon N ( 2018). Ethylene production and signaling in tomato (Solanum lycopersicum) pollen grains is responsive to heat stress conditions. Plant Reprod 31, 367-383. DOI URL
[38]	Kakani VG, Reddy KR, Koti S, Wallace TP, Prasad PVV, Reddy VR, Zhao D ( 2005). Differences inin vitro pollen germination and pollen tube growth of cotton cultivars in response to high temperature. Ann Bot 96, 59-67. DOI URL PMID
[39]	Keller M, Hu Y, Mesihovic A, Fragkostefanakis S, Schleiff E, Simm S ( 2017). Alternative splicing in tomato pollen in response to heat stress. DNA Res 24, 205-217. DOI URL PMID
[40]	Keller M, SPOT-ITN Consortium, Simm S ( 2018). The coupling of transcriptome and proteome adaptation during development and heat stress response of tomato pollen. BMC Genomics 19, 447. DOI URL PMID
[41]	Kim M, Kim H, Lee W, Lee Y, Kwon SW, Lee J ( 2015). Quantitative shotgun proteomics analysis of rice anther proteins after exposure to high temperature. Int J Genomics 2015,238704. DOI URL PMID
[42]	Kotak S, Larkindale J, Lee U, von Koskull-Döring P, Vierling E, Scharf KD ( 2007). Complexity of the heat stress response in plants. Curr Opin Plant Biol 10, 310-316. DOI URL PMID
[43]	Kumar R, Singh AK, Lavania D, Siddiqui MH, Al-Whaibi MH, Grover A ( 2016). Expression analysis of ClpB/ Hsp100 gene in faba bean (Vicia faba L.) plants in response to heat stress. Saudi J Biol Sci 23, 243-247. DOI URL PMID
[44]	Kumar RR, Goswami S, Gadpayle KA, Singh K, Sharma SK, Singh GP, Pathak H, Rai RD ( 2014). Ascorbic acid at pre-anthesis modulate the thermotolerance level of wheat (Triticum aestivum) pollen under heat stress. J Plant Biochem Biotechnol 23, 293-306. DOI URL
[45]	Kumar SV, Wigge PA ( 2010). H2A.Z-containing nucleo- somes mediate the thermosensory response in Arabidopsis. Cell 140, 136-147. DOI URL PMID
[46]	Lang-Mladek C, Popova O, Kiok K, Berlinger M, Rakic B, Aufsatz W, Jonak C, Hauser MT, Luschnig C ( 2010). Transgenerational inheritance and resetting of stress- induced loss of epigenetic gene silencing in Arabidopsis. Mol Plant 3, 594-602. DOI URL PMID
[47]	Larkindale J, Vierling E ( 2008). Core genome responses involved in acclimation to high temperature. Plant Physiol 146, 748-761. DOI URL
[48]	Li N, Zhang DS, Liu HS, Yin CS, Li XX, Liang WQ, Yuan Z, Xu B, Chu HW, Wang J, Wen TQ, Huang H, Luo D, Ma H, Zhang DB ( 2006). The riceTapetum degeneration retardation gene is required for tapetum degradation and anther development. Plant Cell 18, 2999-3014.
[49]	Li SJ, Zhou X, Chen LG, Huang WD, Yu DQ ( 2010). Functional characterization ofArabidopsis thaliana WRKY39 in heat stress. Mol Cells 29, 475-483.
[50]	Li YH, Shen Y, Cai C, Zhong CC, Zhu L, Yuan M, Ren HY ( 2010). The type II Arabidopsis formin14 interacts with microtubules and microfilaments to regulate cell division. Plant Cell 22, 2710-2726. DOI URL PMID
[51]	Liu JZ, Feng LL, Li JM, He ZH ( 2015). Genetic and epigenetic control of plant heat responses. Front Plant Sci 6, 267. DOI URL PMID
[52]	Lobell DB, Schlenker W, Costa-Roberts J ( 2011). Climate trends and global crop production since 1980. Science 333, 616-620. DOI URL PMID
[53]	Lyakh VA, Kravchenko AN, Soroka AI, Dryuchina EN ( 1991). Effects of high temperatures on mature pollen grains in wild and cultivated maize accessions. Euphytica 55, 203-207. DOI URL
[54]	Ma ZX, Leng YJ, Chen GX, Zhou PM, Ye D, Chen LQ ( 2015). The THERMOSENSITIVE MALE STERILE 1 interacts with the BiPs via DnaJ domain and stimulates their atpase enzyme activities in Arabidopsis. PLoS One 10, e0132500. DOI URL PMID
[55]	Mesihovic A, Iannacone R, Firon N, Fragkostefanakis S ( 2016). Heat stress regimes for the investigation of pollen thermotolerance in crop plants. Plant Reprod 29, 93-105. DOI URL PMID
[56]	Migicovsky Z, Yao Y, Kovalchuk I ( 2014). Transgenerational phenotypic and epigenetic changes in response to heat stress in Arabidopsis thaliana . Plant Signal Behav 9, e27971. DOI URL PMID
[57]	Min L, Li YY, Hu Q, Zhu LF, Gao WH, Wu YL, Ding YH, Liu SM, Yang XY, Zhang XL ( 2014). Sugar and auxin signa- ling pathways respond to high-temperature stress during anther development as revealed by transcript profiling analysis in cotton. Plant Physiol 164, 1293-1308. DOI URL PMID
[58]	Mittler R, Finka A, Goloubinoff P ( 2012). How do plants feel the heat? Trends Biochem Sci 37, 118-125. DOI URL PMID
[59]	Müller F, Rieu I ( 2016). Acclimation to high temperature during pollen development. Plant Reprod 29, 107-118. DOI URL PMID
[60]	Ochatt S, Pech C, Grewal R, Conreux C, Lulsdorf M, Jacas L ( 2009). Abiotic stress enhances androgenesis from isolated microspores of some legume species (Fabaceae). J Plant Physiol 166, 1314-1328. DOI URL PMID
[61]	Oliver SN, Dennis ES, Dolferus R ( 2007). ABA regulates apoplastic sugar transport and is a potential signal for cold-induced pollen sterility in rice. Plant Cell Physiol 48, 1319-1330. DOI URL PMID
[62]	Omidi M, Siahpoosh MR, Mamghani R, Modarresi M ( 2014). The influence of terminal heat stress on meiosis abnormalities in pollen mother cells of wheat. Cytologia 79, 49-58. DOI URL
[63]	Oshino T, Abiko M, Saito R, Ichiishi E, Endo M, Kawagishi-Kobayashi M, Higashitani A ( 2007). Premature progression of anther early developmental programs accompanied by comprehensive alterations in transcription du- ring high-temperature injury in barley plants. Mol Genet Genomics 278, 31-42. DOI URL PMID
[64]	Parish RW, Phan HA, Iacuone S, Li SF ( 2012). Tapetal development and abiotic stress: a centre of vulnerability. Funct Plant Biol 39, 553-559. DOI URL
[65]	Parrotta L, Faleri C, Cresti M, Cai G ( 2016). Heat stress affects the cytoskeleton and the delivery of sucrose synthase in tobacco pollen tubes. Planta 243, 43-63. DOI URL PMID
[66]	Paupière MJ, van Heusden AW, Bovy AG ( 2014). The metabolic basis of pollen thermo-tolerance: perspectives for breeding. Metabolites 4, 889-920. DOI URL PMID
[67]	Pecinka A, Scheid OM ( 2012). Stress-induced chromatin changes: a critical view on their heritability. Plant Cell Physiol 53, 801-808. DOI URL
[68]	Pecrix Y, Rallo G, Folzer H, Cigna M, Gudin S, Le Bris M ( 2011). Polyploidization mechanisms: temperature environment can induce diploid gamete formation inRosa sp. J Exp Bot 62, 3587-3597. DOI URL PMID
[69]	Porch TG, Jahn M ( 2001). Effects of high-temperature stress on microsporogenesis in heat-sensitive and heat-tolerant genotypes of Phaseolus vulgaris . Plant Cell Environ 24, 723-731.
[70]	Prasad PVV, Boote KJ, Allen Jr LH, Sheehy JE, Thomas JMG ( 2006). Species, ecotype and cultivar differences in spikelet fertility and harvest index of rice in response to high temperature stress. Field Crops Res 95, 398-411. DOI URL
[71]	Pressman E, Peet MM, Pharr DM ( 2002). The effect of heat stress on tomato pollen characteristics is associated with changes in carbohydrate concentration in the developing anthers. Ann Bot 90, 631-636. DOI URL PMID
[72]	Qi ZY, Wang KX, Yan MY, Kanwar MK, Li DY, Wijaya L, Alyemeni MN, Ahmad P, Zhou J ( 2018). Melatonin alleviates high temperature-induced pollen abortion in Solanum lycopersicum . Molecules 23, 386.
[73]	Qin DD, Wu HY, Peng HR, Yao YY, Ni ZF, Li ZX, Zhou CL, Sun QX ( 2008). Heat stress-responsive transcriptome analysis in heat susceptible and tolerant wheat (Triticum aestivum L.) by using Wheat Genome Array. BMC Genomics 9, 432. DOI URL PMID
[74]	Rahmati Ishka M, Brown E, Weigand C, Tillett RL, Schlauch KA, Miller G, Harper JF ( 2018). A comparison of heat-stress transcriptome changes between wild-type Arabidopsis pollen and a heat-sensitive mutant harboring a knockout of cyclic nucleotide-gated cation channel 16 (cn- gc16). BMC Genomics 19, 549. DOI URL PMID
[75]	Reňák D, Gibalová A, Šolcová K, Honys D ( 2014). A new link between stress response and nucleolar function during pollen development in Arabidopsis mediated by AtREN1 protein. Plant Cell Environ 37, 670-683. DOI URL PMID
[76]	Rezaul IM, Feng BH, Chen TT, Fu WM, Zhang CX, Tao LX, Fu GF ( 2018). Abscisic acid prevents pollen abortion under high-temperature stress by mediating sugar metabolism in rice spikelets. Physiol Plant 165, 644-663. DOI URL PMID
[77]	Saidi Y, Finka A, Muriset M, Bromberg Z, Weiss YG, Maathuis FJM, Goloubinoff P ( 2009). The heat shock response in moss plants is regulated by specific calcium-permeable channels in the plasma membrane. Plant Cell 21, 2829-2843. DOI URL PMID
[78]	Sakata T, Oda S, Tsunaga Y, Shomura H, Kawagishi-Kobayashi M, Aya K, Saeki K, Endo T, Nagano K, Kojima M, Sakakibara H, Watanabe M, Matsuoka M, Higashitani A ( 2014). Reduction of gibberellin by low temperature disrupts pollen development in rice. Plant Physiol 164, 2011-2019. DOI URL PMID
[79]	Sakata T, Oshino T, Miura S, Tomabechi M, Tsunaga Y, Higashitani N, Miyazawa Y, Takahashi H, Watanabe M, Higashitani A ( 2010). Auxins reverse plant male sterility caused by high temperatures. Proc Natl Acad Sci USA 107, 8569-8574. DOI URL
[80]	Sangu E, Tibazarwa FI, Nyomora A, Symonds RC ( 2015). Expression of genes for the biosynthesis of compatible solutes during pollen development under heat stress in tomato (Solanum lycopersicum). J Plant Physiol 178, 10-16. DOI URL PMID
[81]	Sato S, Kamiyama M, Iwata T, Makita N, Furukawa H, Ikeda H ( 2006). Moderate increase of mean daily temperature adversely affects fruit set of lycopersicon esculentum by disrupting specific physiological processes in male reproductive development. Ann Bot 97, 731-738. DOI URL PMID
[82]	Sato S, Peet MM, Thomas JF ( 2002). Determining critical pre- and post-anthesis periods and physiological pro- cesses in Lycopersicon esculentum Mill. exposed to mode- rately elevated temperatures. J Exp Bot 53, 1187-1195.
[83]	Shi WJ, Li X, Schmidt RC, Struik PC, Yin XY, Jagadish SVK ( 2018). Pollen germination andin vivo fertilization in response to high-temperature during flowering in hybrid and inbred rice. Plant Cell Environ 41, 1287-1297. DOI URL PMID
[84]	Snider JL, Oosterhuis DM ( 2011). How does timing, duration and severity of heat stress influence pollen-pistil interactions in angiosperms? Plant Signal Behav 6, 930-933. DOI URL PMID
[85]	Snider JL, Oosterhuis DM, Loka DA, Kawakami EM ( 2011). High temperature limits in vivo pollen tube growth rates by altering diurnal carbohydrate balance in field- grown Gossypium hirsutum pistils. J Plant Physiol 168, 1168-1175. DOI URL PMID
[86]	Solís MT, Rodríguez-Serrano M, Meijón M, Cañal MJ, Cifuentes A, Risueño MC, Testillano PS ( 2012). DNA methylation dynamics andMET1a-like gene expression changes during stress-induced pollen reprogramming to embryogenesis. J Exp Bot 63, 6431-6444. DOI URL PMID
[87]	Song GC, Wang MM, Zeng B, Zhang J, Jiang CL, Hu QR, Geng GT, Tang CM ( 2015). Anther response to high- temperature stress during development and pollen thermotolerance heterosis as revealed by pollen tube growth andin vitro pollen vigor analysis in upland cotton. Planta 241, 1271-1285. DOI URL PMID
[88]	Suzuki K, Takeda H, Tsukaguchi T, Egawa Y ( 2001). Ultrastructural study on degeneration of tapetum in anther of snap bean (Phaseolus vulgaris L.) under heat stress. Sex Plant Reprod 13, 293-299. DOI URL
[89]	Tang RS, Zheng JC, Jin ZQ, Zhang DD, Huang YH, Chen LG ( 2008). Possible correlation between high temperature-induced floret sterility and endogenous levels of IAA, GAs and ABA in rice (Oryza sativa L.). Plant Growth Regul 54, 37-43. DOI URL
[90]	Tunc-Ozdemir M, Tang C, Ishka MR, Brown E, Groves NR, Myers CT, Rato C, Poulsen LR, McDowell S, Miller G, Mittler R, Harper JF ( 2013). A cyclic nucleotide-gated channel (CNGC16) in pollen is critical for stress tolerance in pollen reproductive development. Plant Physiol 161, 1010-1020. DOI URL PMID
[91]	Twell D ( 2011). Male gametogenesis and germline specification in flowering plants. Sex Plant Reprod 24, 149-160. DOI URL PMID
[92]	Verma V, Ravindran P, Kumar PP ( 2016). Plant hormone- mediated regulation of stress responses. BMC Plant Biol 16, 86. DOI URL PMID
[93]	Volkov RA, Panchuk II, Schöffl F ( 2005). Small heat shock proteins are differentially regulated during pollen deve- lopment and following heat stress in tobacco. Plant Mol Biol 57, 487-502. DOI URL PMID
[94]	Wang J, Li DL, Shang FN, Kang XY ( 2017). High temperature-induced production of unreduced pollen and its cytological effects in Populus . Sci Rep 7, 5281. DOI URL PMID
[95]	Ward JM, Mäser P, Schroeder JI ( 2009). Plant ion chan-nels: gene families, physiology, and functional genomics analyses. Annu Rev Physiol 71, 59-82.
[96]	Xing HL, Dong L, Wang ZP, Zhang HY, Han CY, Liu B, Wang XC, Chen QJ ( 2014). A CRISPR/Cas9 toolkit for multiplex genome editing in plants. BMC Plant Biol 14, 327. DOI URL PMID
[97]	Xu JM, Driedonks N, Rutten MJM, Vriezen WH, de Boer GJ, Rieu I ( 2017). Mapping quantitative trait loci for heat tolerance of reproductive traits in tomato (Solanum lyco- persicum). Mol Breed 37, 58. DOI URL PMID
[98]	Yang J, Chen XR, Zhu CL, Peng XS, He XP, Fu JR, Ouyang LJ, Bian JM, Hu LF, Sun XT, Xu J, He HH ( 2015). RNA-seq reveals differentially expressed genes of rice ( Oryza sativa) spikelet in response to temperature interacting with nitrogen at meiosis stage. BMC Genomics 16, 959.
[99]	Yang KZ, Xia C, Liu XL, Dou XY, Wang W, Chen LQ, Zhang XQ, Xie LF, He LY, Ma X, Ye D ( 2009). A mutation in THERMOSENSITIVE MALE STERILE 1, encoding a heat shock protein with DnaJ and PDI domains, leads to thermosensitive gametophytic male sterility in Arabidopsis. Plant J 57, 870-882.
[100]	Zhang CX, Li GY, Chen TT, Feng BH, Fu WM, Yan JX, Islam MR, Jin QY, Tao LX, Fu GF ( 2018). Heat stress induces spikelet sterility in rice at anthesis through inhibition of pollen tube elongation interfering with auxin homeostasis in pollinated pistils. Rice 11, 14. DOI URL PMID
[101]	Zhang DB, Luo X, Zhu L ( 2011). Cytological analysis and genetic control of rice anther development. J Genet Genomics 38, 379-390. DOI URL PMID
[102]	Zhang W, Zhou RG, Gao YJ, Zheng SZ, Xu P, Zhang SQ, Sun DY ( 2009). Molecular and genetic evidence for the key role of AtCaM3 in heat-shock signal transduction in Arabidopsis. Plant Physiol 149, 1773-1784. DOI URL
[103]	Zhao Q, Zhou LJ, Liu JC, Cao ZZ, Du XX, Huang FD, Pan G, Cheng FM ( 2018a). Involvement of CAT in the detoxification of HT-induced ROS burst in rice anther and its relation to pollen fertility. Plant Cell Rep 37, 741-757. DOI URL PMID
[104]	Zhao Q, Zhou LJ, Liu JC, Du XX, Asad MAU, Huang FD, Pan G, Cheng FM ( 2018b). Relationship of ROS accumulation and superoxide dismutase isozymes in develop- ping anther with floret fertility of rice under heat stress. Plant Physiol Biochem 122, 90-101. DOI URL PMID
[105]	Zinn KE, Tunc-Ozdemir M, Harper JF ( 2010). Temperature stress and plant sexual reproduction: uncovering the wea- kest links. J Exp Bot 61, 1959-1968. DOI URL